Gene Transposition as a Cause of Hybrid Sterility in
            <i>Drosophila</i>

Masly, John P.; Jones, Corbin D.; Noor, Mohamed A. F.; Locke, John; Orr, H. Allen

doi:10.1126/science.1128721

Cited by 190 publications

(153 citation statements)

References 20 publications

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“…Indeed, QTL size (7.35% PVE) was at the detection limit despite the large size of the QTL population. This contrasts with recent studies in Drosophila, where several genes have recently been cloned that cause almost complete reproductive isolation (Tinget al 1998;Barbash et al 2003;Presgraves 2003;Masly et al 2006). Likewise, major QTL for sterility are frequently detected in flowering plants (Moyle and Graham 2005;Fishman and Willis 2006;Sweigart et al 2006).…”

Section: Mechanisms Of Reproductive Isolationcontrasting

confidence: 45%

A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern,Ceratopteris richardii

et al. 2007

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Biological factors involved in reproductive barriers between two divergent races of Ceratopteris richardii were investigated. We used a combination of spore germination rates, QTL analysis of spore germination rates, and transmission ratio distortion (TRD) of 729 RFLPs, AFLPs, and isozyme markers distributed across the genome on the basis of hybrid populations of 488 doubled haploid lines (DHLs) and 168 F 2 's. Substantial reproductive barriers were found between the parental races, predominantly in the form of spore inviability (23.7% F 1 spore viability). Intrinsic genetic factors such as Bateson-Dobzhansky-Muller (BDM) incompatibilities involving both nuclear-nuclear and nuclear-cytoplasmic factors and chromosomal rearrangements appear to contribute to intrinsic postzygotic isolation. The genomewide distribution patterns of TRD loci support the hypothesis that reproductive barriers are a byproduct of divergence in allopatry and that the strong reproductive barriers are attributable to a small number of genetic elements scattered throughout the genome.

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Section: Mechanisms Of Reproductive Isolationcontrasting

confidence: 45%

A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern,Ceratopteris richardii

et al. 2007

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“…Duplication and differentiation between paralogs can alter the genetic architecture of male and female traits, and hybridization between species can potentially disrupt the transmission of sex-specific genes, leading to sex-specific hybrid inviability or sterility (see Lynch and Force 2000;Masly et al 2006). Gene duplication between chromosomes, particularly the movement of male functions from the X to the autosomes, can disproportionately affect males and might partially account for the two rules of speciation (Moyle et al 2010): ''Haldane's rule'' (Haldane 1922;Coyne and Orr 2004) and the ''large-X effect'' (Coyne and Orr 1989;True et al 1996;Tao et al 2003;Masly and Presgraves 2007;Presgraves 2008).…”

Section: Discussionmentioning

confidence: 99%

The Resolution of Sexual Antagonism by Gene Duplication

2011

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Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic ''tug-of-war'' that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes-within the explicit context of duplication and sexual antagonism-has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.

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“…Advanced crosses using sophisticated genetic trickery (i.e., X-ray irradiation or hybrid rescue mutations) to overcome F 1 isolation have shown that hybrid male sterility is highly polygenic and complex (Pontecorvo 1943;Sawumura et al 2000). Indeed, even the tiny dot chromosome causes hybrid male sterility in these species (Muller and Pontecorvo 1940;Masly et al 2006). In marked contrast, only a few QTL contribute to hybrid male sterility between D. virilis and D. americana, two species distinguished by roughly the same degree of synonymous genetic divergence as D. melanogaster and D. simulans (D. virilis-D. americana K s 0.11, MoralesHojas et al 2008).…”

Section: Discussionmentioning

confidence: 99%

“…A recent survey of Y-linked genes among the 12 sequenced Drosophila species found low conservation of gene content (Koerich et al 2008). If gene movement on and off the Y chromosome has occurred repeatedly in the D. virilis group, crosses between species might yield hybrids that lack a full complement of essential male fertility factors (see Masly et al 2006;Lynch and Force 2000). To investigate this possibility, I designed primers to PCR amplify an exon from each of the six genes known to be Y-linked in D. virilis (kl-2, kl-3, kl-5, ORY, PPr-Y, and PRY: see Koerich et al 2008).…”

Section: Discussionmentioning

confidence: 99%

Simple Y-Autosomal Incompatibilities Cause Hybrid Male Sterility in Reciprocal Crosses Between Drosophila virilis and D. americana

Sweigart

2010

Genetics

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Postzygotic reproductive isolation evolves when hybrid incompatibilities accumulate between diverging populations. Here, I examine the genetic basis of hybrid male sterility between two species of Drosophila, Drosophila virilis and D. americana. From these analyses, I reach several conclusions. First, neither species carries any autosomal dominant hybrid male sterility alleles: reciprocal F 1 hybrid males are perfectly fertile. Second, later generation (backcross and F 2 ) hybrid male sterility between D. virilis and D. americana is not polygenic. In fact, I identified only three genetically independent incompatibilities that cause hybrid male sterility. Remarkably, each of these incompatibilities involves the Y chromosome. In one direction of the cross, the D. americana Y is incompatible with recessive D. virilis alleles at loci on chromosomes 2 and 5. In the other direction, the D. virilis Y chromosome causes hybrid male sterility in combination with recessive D. americana alleles at a single QTL on chromosome 5. Finally, in contrast with findings from other Drosophila species pairs, the X chromosome has only a modest effect on hybrid male sterility between D. virilis and D. americana.

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Gene Transposition as a Cause of Hybrid Sterility in Drosophila

Cited by 190 publications

References 20 publications

A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern,Ceratopteris richardii

A Genomewide Study of Reproductive Barriers Between Allopatric Populations of a Homosporous Fern,Ceratopteris richardii

The Resolution of Sexual Antagonism by Gene Duplication

Simple Y-Autosomal Incompatibilities Cause Hybrid Male Sterility in Reciprocal Crosses Between Drosophila virilis and D. americana

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